Chapter 1. Linking Function between Scales of Resolution

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fundamental question is still relevant today. Ecosystem function is not governed by the

species of fungi present, but by the role that each fungus plays in carrying out certain

tasks and the rates at which these tasks are accomplished. Future research needs to link

diversity and function. Much of the current literature that addresses microbial community

dynamics does not differentiate between the relative contributions of fungal communities

and bacterial communities. We thus have a poor understanding of both the specific role

of fungi in general and the specific roles of individual species for most ecosystem

processes in which they participate. By definition, this is a scalar issue: fungi act on

individual molecules at microscopic scales, yet aggregate effects are felt at ecosystem

and landscape scales. In this chapter we first present ecological questions that mycologists

are not now adequately addressing and then focus on the tools needed to adequately

evaluate soil fungal communities.



1.2



ECOLOGICAL SCALE



1.2.1

Linking from Molecules to Individuals

Molecular signaling plays a large role in directing the life cycle and functions of fungi.

Evaluating the response of fungi to external stimuli, including dormancy, germination,

resource acquisition, sporulation, and dispersal, requires an understanding of the molecular

cues that signal appropriate timing for each of these events. For evaluating soil fungi, the

cues for dormancy or for germination are a sufficient start for tying molecular level

processes to individual behavior. More important, perhaps, are the cues that signal positive

interactions, such as the formation of mycorrhizas, and negative interactions, such as

staving off attacks by pathogens. Advances have identified some of these cues, e.g.,

alterations in nutrient content, light, aeration, temperature, pH, and activity of phenols and

polyphenoloxidases (Andrews and Harris, 1997), but the fine-scale work to examine what

promotes these activities in the natural environment lags behind laboratory work that may

not adequately represent in vivo conditions. Simplistic approaches are valuable for identifying potentially important interactions but necessarily ignore complex species–species

interactions such as multitrophic signals in the rhizosphere. These can be of great importance, a consequence of the long coevolutionary history among rhizosphere organisms

(Phillips et al., 2003). Knowledge of the extent of these molecules exist and of the processes

they control is necessary for evaluating rhizosphere control points and, more importantly,

for interpreting consequences of anthropogenic disturbance for belowground communities.

Molecules used for food acquisition are as important as signaling molecules. Measurements of exoenzymes have begun to provide important information on the activity of

soil microfungi and the resources that they are consuming, but there is yet little linkage

to the types and numbers of fungal species that produce the enzymes. The reduction of

competition for food resources is also mediated by the production of antimicrobial or

antifungal compounds that affect species distribution at small scales. Of particular interest

are the molecules used by ectomycorrhizal (EM) fungi for capturing nutrient resources.

For example, predation upon live collembolan (Klironomos and Hart, 2001) or dead

nematodes (Perez-Moreno and Read, 2001) in soil by EM fungi allows for a much more

direct route of nutrient acquisition. These pathways are likely driven by enzymatic activities

that can be detected at the molecular level in soils. Determining whether other fungi are

capable of deriving nutrients directly from organisms in the soil food web is necessary to

complete linkages in nutrient cycles, fully evaluate the impacts of species loss, and allow

for an understanding of the evolution of these traits and their relevancy in terms of overall

nutrient cycling in soils.



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Identifying the molecules that affect and are affected by fungi is essential. Determining the degree to which molecules influence multiple trophic levels or affect synergistic

activities is also important. Identifying the spatial scale at which these molecules work,

their patterns of temporal production, and their longevity is significant for evaluating the

impact of these molecules on overall community dynamics.

1.2.2

Linking from Individuals to Communities

Overall, the diversity of soil fungi is immense, with current projections at 1.5 million

species (Hawksworth, 1991). The unique genetics of fungi, including homo- vs. heterokaryotic organisms, allow for molecular control of mechanisms that differ from other

organisms and allows genetic diversity to be preserved and increased in unusual ways.

Population characteristics of fungi are influenced by their unique genetics. For example,

the short dispersal distances of fungi would suggest that there might be low genetic

diversity within populations, yet research by Vandenkoornhuyse et al. (2001) suggests that

this may not be the case: specific fungal groups may have a much greater intrapopulation

genetic diversity than interpopulation diversity. Müller et al. (2001) detected greater

diversity within populations for endophytes than for saprophytes on the same tissue.

Villeneuve et al. (1989) found that mycorrhizal species richness is relatively constant along

a gradient of environmental disturbance, while saprophytic fungal diversity decreases along

the same gradient.

High genetic diversity within populations may be instrumental to the ease with which

fungi have evolved mutualistic relationships in multiple groups. The extremely high levels

of variation in small arbuscular mycorrhizal (AM) populations suggest that mechanisms

for recombination have been underestimated in fungi and recombination rates may actually

be enhanced by changes in environmental conditions to which fungi are exposed (Vandenkoornhuyse et al., 2001). This has been extremely difficult to study in field trials.

Laboratory studies are now beginning to confirm that genetic diversity of fungi in soil

environments is much higher than fungal diversity of organisms found in laboratories

(Castelli and Casper, 2003). Greater ties among population dynamics such as genetic

structure, spatial distribution of individuals vs. hyphal networks or spores, and the relative

age structure of populations would contribute greatly to defining the role of individual

species in community interactions.

Increased understanding of genetic diversity in soil fungi is also essential to evaluate

the degree to which there is true functional redundancy. While great strides have been

made in identifying organisms, especially since the increased availability of molecular

tools, tying specific organisms to specific processes in the complex environmental matrix

of soil is still lagging (Gray et al., 2001). Examinations of AM and EM fungi as a functional

group have indicated that mycorrhizal fungi respond directly to environmental cues,

independently of their plant host (Allen et al., 1995). Research indicates that there is high

functional diversity in mycorrhizal fungi within and across habitats, and should there be

loss of fungal species, there will be a significant shift in how plants acquire resources in

specific habitats. More studies that tie genetics to function are necessary to evaluate the

degree to which loss of genetic diversity will affect the resistance or resilience of ecosystems following global climate change. Identifying individual species and responses to

environmental cues is essential to evaluating the roles and interactions of fungal species

in terrestrial communities.

1.2.3

Linking from Communities to Ecosystems

Fungi play multiple roles in terrestrial communities as saprotrophs, predators, and pathogens and as mutualists of photosynthetic organisms (lichen, mycorrhizas). Fungi can be



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endophytes on leaves that fall from trees and then become part of decomposer communities. They are key components of soil food webs as consumers, predators, pathogens, and

decomposers. Few would argue that their contributions to community dynamics are not

important to the organization and structure of terrestrial systems. Exploring the interactions

of fungi within the fungal community and their role in determining plant communities,

especially as decomposers and mutualists, has highlighted the fact that fungi are intimately

involved with components of energy acquisition and distribution.

Fungal pathogens can play a large role in maintaining plant species diversity. Pathogens can influence the success of a given species by allowing it to coexist with other

species (Westover and Bever, 2001), or pathogens can cause the loss of a species by

decreasing its competitive ability, allowing its replacement during succession (Van der

Putten and Peters, 1997), during competition, or following disturbance. These relationships

can be difficult to detect, as some interactions among pathogens and synergisms with

mutualists can depend on life stage (Smith and Read, 1997). Pathogens can also play a

role in tree species diversity and in the spatial distribution of species (Packer and Clay,

2000; Reinhart et al., 2003). Mortalities of black cherry seedlings were very high under

soil collected from under black cherry, but not from 30 m away, due to a pythium species

that prevented seedling establishment. This inhibition was alleviated when black cherry

was introduced in an area without pythium.

A great deal of research has addressed the impacts of mutualists on plant community

structure. Plant diversity is promoted by mutualists that supply nutrients to plants that

would otherwise be poor competitors. Some of this research suggests that diversity can

be increased only if AM fungi are heterogeneously distributed or if benefits to plant species

differ (Jordan et al., 2000). Differences in the efficiency of resource capture by mycorrhizal

fungi and the resultant impact on plant growth have been demonstrated many times (Van

der Heijden et al., 1998a; Klironomos, 2003). The impact of mycorrhizae on its host can

range from that of a parasite to that of a mutualist. The consequence is differential impacts

on host species with concomitant effects on aboveground species diversity.

Little attention has been focused on the impact of belowground diversity on aboveground function. Baxter and Dighton (2001) found that increasing fungal diversity

decreased shoot growth of grey birch and increased mycorrhizal root length. This suggests

a decrease in benefit for plants with increased mycorrhizal diversity. In contrast, Klironomos et al. (2000) found an asymptotic increase in net primary production (NPP) with the

addition of belowground species. The increases in plant productivity with added aboveground diversity found by others, such as Tilman et al. (1997), were not mirrored by an

increase in plant productivity with increased belowground diversity. The addition of only

two mycorrhizal species saturated the productivity curve.

In addition to impacts on aboveground plant diversity, mycorrhizal fungi can also

influence other communities such as insects. Gange (2001) found that a single mycorrhizal

fungi decreased larval survival and biomass of the root-feeding black vine weevil, whereas

colonization by two mycorrhizal fungi did not. Similarly, Gange et al. (1994) demonstrated

that the presence of mycorrhizae on the roots of Taraxacum officinale decreased the number

of black pine weevil larvae feeding on the roots. Both ecto- and endomycorrhizal species

have been reported to protect plant hosts from pathogenic attack (Azcon-Aguilar and

Barea, 1992).

1.2.4

Linking from Ecosystem Scales to Global Scales

Read and Perez-Moreno (2003) have suggested that mycorrhizal fungi may provide a

crucial link between communities and ecosystems. The relationship integrates above- and

belowground dynamics as the response variable for nutrient cycling and decomposition



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and is a rate-limiting step that can influence both net primary productivity and tissue

quality. Cornelissen et al. (2001) compared plants of known functional and mycorrhizal

type and found that mycorrhizal strategies are linked to productivity and litter turnover.

The physiological potential of each mycorrhizal group (AM, EM, ericoid) may allow for

the development of a mechanistic understanding of distinctive plant communities across

local to regional scales.

Modeling allows a mechanism for linking ecosystem level processes with real-world

scenarios. These models are useful for predicting changes in global scale patterns due to

changes in ecosystem level processes and for understanding the impact of abiotic change

on biotic communities and feedbacks between the two. Fungi have been incorporated into

these models as components of nutrient turnover, but rarely as more than a black box.

Because the most important indicators of microbial activity at the global scale are moisture

and temperature, the role of fungi as decomposers is often included as a simple rate

function or as a component of organic matter turnover. These models have capabilities

necessary for predicting changes to nutrient turnover under differing scenarios of global

climate change, land use change, or alterations to system management, but are not adequate

to evaluate changes to ecosystem components if alterations result in changes in fungal

species that affect ecosystem energy acquisition or species diversity.

Hunt and Wall (2002) specifically modeled the effect of species loss on net primary

productivity and found that the deletion of only two groups, saprophytic fungi and bacteria,

caused large changes in net primary productivity. This suggests that as a group, fungi are

not redundant, nor are they functionally interchangeable with bacterial decomposers.

Much would be gained from including fungi as a group in modeling efforts, but first,

specific model parameters must be created and evaluated, and specific values for contributions of mutualists, saprophytes, pathogens, and predators need to be derived. To achieve

the goals of linking individuals to communities and to link these roles in a quantitative

fashion to ecosystem dynamics require tools appropriate to different scales.



1.3



PHYSICAL SCALE



Fungi are spatially structured in soils in response to a number of biotic and abiotic features

(Ettema and Wardle, 2002). At the smallest scales, fungi respond to soil pores, aggregates,

particulate organic matter, and fine roots. They are also structured in response to vegetation

patterns such as size, spacing, root distribution, and the distribution of vegetative resources

such as exudates, leaf litter, stem flow, and throughfall. At larger spatial scales, fungi are

structured by soil type, land use, topography, and microclimate. At global scales, they are

affected by climate and by anthropogenic disturbances such as pollutants. Integrating

across physical scales is necessary to integrate fungal dynamics across ecological scales.

The current approach to understanding fungal ecology is limited by the techniques and

approaches currently available.

1.3.1

Linking from the Microscale to the Plot Scale

At the microscale, current methodology for sampling fungi is limited. Evaluating mechanisms by which fungi acquire their resources at a scale relevant to the organisms themselves has been difficult in the field under natural conditions. The recent development of

techniques that allow for the in vitro evaluation of organisms under laboratory conditions

on native substrates is providing data that will allow us to more easily transfer studies

from laboratory to field situations. Resources can now be tied to the organisms responsible

for decomposition in such a manner that changes in chemistry and organisms can be



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followed simultaneously. For example, litter carbohydrate availability has been tied to the

advancing mycelial front by microscopic Fourier transform infrared spectroscopy (Dighton

et al., 2001). This process allows fungal succession to be plotted against specific changes

in substrate chemistry. Ultimately, fungal succession can then be tied to process level

mechanisms.

In addition to determining the interface between resources and organisms, it is also

essential to determine the location of the substrate and the distance over which nutrients

travel. Gaillard et al. (1999) demonstrated changes in microbial heterogeneity by following

13C and 15N concentrations in soil. Movement of materials up to 4 mm away from the

labeled substrate was attributed to transport through fungal hyphae growing on the substrate. This distance begins to define what is now considered the detritusphere and should

begin to suggest the size of the feeding zone relevant to fungi. Developing techniques for

evaluating the relationship between hyphal development, nutrient acquisition, and transport

distance should allow mechanistic investigations of decomposition dynamics to be linked

to species diversity. Quantitative analyses of mechanisms by which fungi acquire resources

and participate in nutrient cycling are necessary to link diversity and abundance to specific

ecological roles.

There are few approaches available to study intact fungal communities. Culture work

only allows for isolation of individual fungi, and few organisms can be manipulated this

way. Community studies using this technique provide little understanding of the role of

fungal biomass or diversity in soil. Collecting fungal hyphae or spores from soil cores for

cultures fails to preserve hyphal networks, destroys linkages between fungi and other

organisms, and obscures the extent to which the fungi affect ecosystem function in soil

systems. Measurements of hyphal lengths can indicate the presence of a fungus at some

time in the past, or they can indicate the presence of an active fungus, depending on the

techniques used. In either case, such measurements do not indicate the activity of the

organism, its age, or its identity.

Not all hyphae are equal in function, contribution to soil dynamics, or community

structure. Fungal hyphae can be differentiated based on a number of characteristics. Prior

to the development of molecular techniques, hyphae were distinguished based on physical

characteristics, and this provided information on a number of interactions of specific hyphae

in soils. For example, differentiating hyphae based on color alone increased the understanding of the differential preference of fungi as a food source for microarthropods

(Klironomos and Kendrick, 1995a). Lab feeding trials had suggested that collembolan

prefer mycorrhizal fungi, yet field observations of coloration led Klironomos and Kendrick

(1996) to suspect a larger role for pigmented fungi on decaying litter, which was confirmed

by more elaborate feeding trials. This illustrates the degree to which our understanding of

small-scale dynamics can be obscured by moving organisms out of their native soil matrix.

The rate at which hyphae are produced and retired in soils has been poorly quantified.

Recently, Staddon et al. (2003) detected hyphal turnover rates for AM fungi suggesting

that extraradical hyphae turn over on average every 5 to 6 days. Turnover this rapid makes

hyphae a very rapid conduit by which C is supplied directly to belowground systems from

plant photosynthesis. Additionally, Rillig et al. (2003) found correlations between AM

mycoproteins and a soil C pool of significant size and relatively slow turnover rates. As

hyphae and products of fungal growth have significant impacts on local soil C pools, they

should be included in examinations of global C cycles.

Fungi as saprophytes, mutualists, and pathogens are involved in hyphal networks

that connect them to nutrient sources and water, form bridges between plant species,

participate in sporulation, form aggregates, and provide for invasions of uncolonized areas.

Fungal hyphal networks can also function in nutrient transfers in the soil. The simplistic



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source–sink transfer hypothesis has been replaced by a bidirectional translocation hypothesis sparked by studies on wood decay fungi (Connolly and Jellison, 1997; Lindahl et al.,

2001). Frey et al. (2003) found that fungi transfer litter-derived C to soil macroaggregates

while transferring soil-derived N to the litter layer. Carbon and nitrogen pools are altered

by fungi across spatial scales and thus need to be examined at a level that allows mechanisms of plant support, soil building, and litter decomposition to be linked.

Fungal hyphal lengths correlate with a number of soil physical, chemical, and

biological properties. Yet it is nearly impossible to determine the individual species or the

distinct activities that result in functions such as decomposition, nutrient transfer, or host

protection against pathogens or predators. Fortunately, molecular techniques are affording

mycologists the opportunity to examine the species represented by hyphae, but they do

not begin to provide answers to the extent or organization of fungal hyphal networks in

soil. This alone would allow for the design of better and more functional sampling schemes

and for understanding of the role of fungi in community and ecosystem dynamics.

Alternately, we can follow fungal spore production or appearance of fungal fruiting

bodies. While we can quantify the production of spores, the temporal and spatial aspects

of spore production are poorly understood. The timing and location of fungal sporulation

relative to the hyphal network, nutrient supply, host, or some other stimuli are still

important questions that need to be more fully addressed. Relating the appearance of

spores or fruiting bodies to ecosystem dynamics also has its drawbacks because the rate

of sporulation or production of fruiting bodies cannot be linked quantitatively to specific

ecosystem characteristics. That sporocarps are produced indicates the presence of a belowground fungus, yet the presence of a belowground fungus is not always indicated by an

aboveground sporocarp (Gardes and Bruns, 1996; Dahlberg et al., 1997). Additionally,

production of sporocarps may not be related to the relative abundance of colonization of

EM on roots (Clapp et al., 1995). Similar problems are encountered when characterizing

the AM community based on spore counts (Bever et al., 1996, 2001). While measuring

diversity or biomass may not be hampered by these results, scaling up to impacts on

community structure or evaluating global climate-change effects cannot be achieved without linking spores to fungal function.

Spore counts are also difficult to evaluate because spores tend to have clumped

distributions, which may cause diversity measures to change dramatically, depending on

where samples are taken. The diversity of fungal spores in soil initially or following a

single trapping period also may not reflect all of the species present and may be affected

by the plant host. Multiple techniques are necessary to evaluate mycorrhizal species

diversity under field conditions.

Studies that have examined fungi at the microscale have found patterning at this

scale. Patterns of active fungal hyphal lengths were linked to vegetation patterns, topography, organic C, and moisture at small spatial scales (<1 m) (Morris, 1999). The patterns

detected in microplots suggested hot spots of microbial activity that were approximately

2 cm in diameter. This was consistent with a number of other studies (Starr et al., 1992;

Gonod et al., 2003), suggesting that high variation can be introduced into data sets if

samples are not homogenized prior to analysis. This also means that mechanistic studies

for identifying the impact of community structure and abiotic factors must be performed

at the centimeter scale, whereas data for scaling up must be performed on composited

samples that decrease the “noise” generated by differences in response to soil resource

heterogeneity.

An additional difficulty in determining the microscale distribution of fungi in soils

is the impact that they have on the microscale patterning of soils. For example, the presence

of fungal hyphae has been linked to formation of water-stable macroaggregates, which is



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important for protecting soil organic matter and improving soil structure (Denef et al.,

2001). The mechanism by which fungi accomplish this task is obscured by poor understanding of spatial structure of bacterial vs. fungal populations, the species of fungi

involved in aggregate formation, and differential impacts of wet–dry cycles on these

organisms. Information on the distribution of fungi within aggregates, i.e., at the smallest

spatial scales in soil, would provide valuable data on the importance of the presence of

hyphae in organic matter stabilization, nutrient retention, soil stability, and soil structure.

Different communities may also be involved with decomposition associated with different

aggregate fractions or soil structural classifications (light fraction vs. particulate organic

matter dynamics). Understanding these dynamics is essential for evaluating the roles of

fungi in organic matter turnover in soils.

Microscale patterns suggest differences in fungal distribution at the millimeter scale.

At the centimeter scale the distribution of fungi is also impacted by litter and soil depth.

Sampling through a profile will identify different groups of organisms at different depths.

Some studies have found that the degradative capacities of these organisms may not differ

much from groups at other depths (Bååth and Söderström, 1980). Differences in consumption of fungal hyphae by soil organisms are also affected by the distribution of hyphae.

Hyphal lengths in the litter layer are even more susceptible to faunal feeding than hyphae

in lower layers (Klironomos and Kendrick, 1995b). Removal of the litter layer alters

consumption patterns and density of fungal hyphae. When litter layers are removed, fungal

feeders spend more time consuming mycorrhizal fungi than litter fungi. This may decrease

the hyphal network of the fungus. The degree to which the extraradical hyphal network

is necessary for mycorrhizal function and the length of time that it is active are currently

unknown. This information is necessary to evaluate the impact of the fungal feeders on

mycorrhizal functioning and NPP.

Advances using molecular techniques have also identified EM fungi distributed

across different soil layers. Niche differentiation across soil substrates has been proposed

to contribute to EM diversity. The research presented by Dickie et al. (2002) supports this

hypothesis and detected, even with relatively shallow sampling, up to six different patterns

of spatial resource partitioning from the four layers sampled (lower litter, fermentation

layer, humified layer, and B horizon (2 cm below the humified layer). The results of Taylor

and Bruns (1999), using molecular techniques, also identified differences in patterns among

both the mature forest community and the resistant propagule community in a Pinus

muricata forest. Their results demonstrated differences in resource preferences and colonization strategy for maintaining species richness in the EM community. These improved

identification methods and microscale approaches will allow for better understanding of

the distribution of fungi in soils. Ultimately, distribution patterns are influenced by more

than just physiology and abiotic factors; the role of biotic patterns must also be determined.

Approaches that strive to incorporate an understanding of the ecological roles that fungi

play will likely result in data that will improve our understanding of fungi in ecosystems

and improve our ability to design sampling schemes for studying these organisms.

Many studies have examined the scale at which other soil organisms (e.g., Robertson

and Freckman, 1995) and other microbial community parameters (Arah, 1990; Boerner et

al., 1996; Decker et al., 1999) exist in soils. The distributions of these organisms, which are

tied to fungi through trophic or competitive interactions, contribute to the spatial distribution

of fungi in soils. Studies have reported correlations between the distributions of these

organisms in soil and interactions between specific groups. Specifically, increases in hyphal

length are associated with fungal grazing by arthropods (Hanlon, 1981; Hedlund et al.,

1991) through removal of inhibitory compounds and senesced fungal materials. Fungi have

also been observed to increase arthropod fecundity (Klironomos et al., 1992). Belowground



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communities are as complex as any aboveground food web but are even more difficult to

study, as identity of the participants and system feedback loops are often obscured. Microscale studies are needed to examine soil food web dynamics at the scale at which they operate

in intact systems or through studies that include as many of the complex interacting groups

of organisms as possible in greenhouse or common garden experiments.

The assumptions currently made for individuals and their impacts at higher scales

are those of linearity (Bever, 2003). Yet there is evidence of nonlinear feedback from the

microbial community to the plant community. To scale from individuals to plot scale

studies an understanding of the degree to which these assumptions can be made must be

examined. We also need information on the degree to which the feedback mechanisms of

the microbial community, both negative and positive, operate simultaneously to impact

species presence in plant communities.

1.3.2

Linking from the Plot Scale to the Landscape Scale

The experimental unit for studying fungi or changes in microbial community dynamics

in response to some treatment is often the plot or, in larger studies, the watershed. To

adequately address research questions regarding fungi, sampling schemes at this scale

must be representative of the organisms studied. Stratifying sampling schemes to include

the parameters that most likely affect fungi is important. The impact of vegetation has

been documented in a number of studies (Zinke, 1962; Morris, 1999), as has topography

(Morris and Boerner, 1999). The latter is not surprising, as topography is often associated

with moisture. Incorporating positional impacts of landscape components into sampling

schemes increases the probability of decreasing random noise and improves the probability

of detecting treatment differences when they exist.

Problems that may confound the ability to detect differences even after constraining

for these variables are the local scale differences in fungal biomass that may not be

accounted for at either local (vegetation) or regional scales. Contiguous watersheds, which

are often used as treatment units, may be problematic for studying treatment impacts on

fungi. One study that examined microbial community dynamics in southern Ohio found

that while bacterial biomass pretreatment differed only across regions, fungal biomass

differed across watersheds within a region (Morris and Boerner, 1999). The strongest

predictors for fungal biomass were sand, clay, and long-term indicators of moisture patterns

(e.g., slope, aspect, water-holding capacity), suggesting that fungal biomass was subject

to intermediate-scale impacts that increase random noise across otherwise homogenous

watersheds. Better ways to quantify fungal biomass, specifically for understanding the

value of fungal hyphal lengths, are necessary to evaluate the impacts of treatments on fungi.

Fungi also differ in energy contributions to different fungal structures. Studies that

examined the relative contributions of AM fungi to intraradical and extraradical hyphae,

arbuscules, and hyphal coils found soil nutrient content to affect contributions to each of

these structures (Johnson et al., 2003). While this approach ties structure to function, it

suggests that studies that compare fungal hyphal lengths across different sites may confound locational or treatment effects by negating the contributions of small-scale differences in nutrient content on hyphal production. Treseder and Allen (2002) found changes

in hyphal length following nutrient additions to be related to current site nutrient limitations

and species present. These results suggest that pretreatment dynamics in fungal studies

can be even more important than for other types of organisms.

Multiple studies have suggested that even at local scales fungi are elusive. Studies of

a single-hectare abandoned agricultural site have yielded an unprecedented 37 species of

AM fungi only after years of study using multiple approaches (Bever et al., 2001). Conventional wisdom suggests that this site should have had a low diversity of fungi directing



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a high diversity of plants. These misconceptions permeate the literature and limit our ability

to clarify the number of fungal species even across a single hectare. Acquiring accurate data

on species numbers is essential to understanding diversity. This step must precede development of hypotheses on the mechanisms that drive diversity of these organisms.

1.3.3

Linking from the Landscape Scale to Global Scale

While differences within study areas may be difficult to detect, there has been great success

identifying differences in communities as we move across landscapes. Taylor and Bruns

(1999) found differences in the community structure of EM fungi in a Pinus muricata

forest and demonstrated minimal overlap in two different groups of fungi across a disturbance gradient. Boerner et al. (1996) demonstrated differences in spatial patterns across a

gradient from native systems to agricultural systems. Their results suggested that the

distribution of AM propagules became more homogenous with an increase in age since

disturbance. This is even more important for evaluating EM infectiveness following disturbance. Five years after disturbance, the probability of an EM-dependent seedling encountering EM inoculum was only 50%. This increased to 100% 25 to 30 years after disturbance.

Landscape patterning is important to evaluate because the distance to inoculum affects

the recolonization of fungi and, thereby, plants. Recovery of vegetation following the

volcanic disturbance at Mt. St. Helens was slowed by poor inoculum density and likely poor

distribution of EM mating types on the most severely disturbed sites (Allen et al., 1992).

Twenty years after the volcanic blast, poor development of conifers at the site is likely the

consequence of the number of years spent without appropriate inoculum and the poor

distribution of nutrients. Low inoculum density affected plants that associate with AM fungi

less severely because they are often facultative and AM fungi have larger spores that may

be more easily distributed by fossorial mammals and animals located in refugia. Evaluating

the impact of landscape mosaics on distribution patterns and availability of fungi is necessary

to predict recovery following disturbances, including large-scale climate change.

It is one thing to discuss the roles of fungi at each scale, but how does one approach

integrating across scales to understand the overall global contribution of fungi? Plot level

studies must incorporate microscale patterning in a representative way. To adequately

achieve this goal, we must be able to provide information on fungal distribution patterns.

We cannot currently evaluate the degree to which our methodologies are adequate to detect

all of the fungi and organisms that interact with the fungi in a single gram of soil.

Mycologists have begun to identify the incremental increase in NPP contributed by

mycorrhizal relationships (i.e., the contributions to aboveground and belowground food

webs), but integrating the affiliated changes in plant chemistry with decomposition rates

is now necessary to evaluate the impact of the mycorrhizal relationship on overall ecosystem dynamics. Additionally, changes in diversity of aboveground species will also

contribute to alterations in NPP. How can this contribution be quantified if not at the

individual plant scale? Mycorrhizal fungi may be a key link for understanding the tie

between atmosphere and plant growth and will likely be an essential driver for evaluating

the impacts of elevated CO2 on terrestrial systems (Fitter et al., 2000). In this same way,

the impacts of temperature change on decomposer fungi will likely be key to understanding

feedback mechanisms in terms of nutrition and CO2 concentrations in ecosystems.



1.4



CONCLUSIONS



Microscale patterning of soil organisms results in what is perceived as random noise when

sampled at small scales (Ettema and Wardle, 2002). This is a problem for identifying the



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fungal contribution to overall ecosystem function. It is essential to begin to establish the

source of the noise and identify the roles of individuals and the spatial dynamics that allow

them to perform these roles. Additionally, the difficulty of evaluating the composition of

the microbial community and apparent simplicity with which it can be modeled has caused

microorganisms of all varieties to be considered functionally redundant and, therefore, of

little concern at the species or microscale level. While this may work currently for global

scale modeling, failure to elucidate the contributions of individual species to the structure

of communities and functioning of ecosystems will limit our ability to predict impacts of

global climate change, anthropogenic disturbance, or habitat fragmentation on the resistance or resilience of ecosystems. To this end we have the following research needs:

1.

2.

3.

4.

5.



To

To

To

To

To



elucidate the role of specific fungi in contributions to functional processes

connect hyphal networks to their function

relate hyphal networks to spore counts

unite DNA technologies with indices that indicate activity

provide linkages across scales to other organisms in the food web



The concern of Waksman (1916) that who is active is more important than who is present

has not been adequately addressed even today. However, with the advent of molecular

techniques and the speed with which they have already transformed our knowledge of

belowground fungal communities, we are now in a much better position to answer the

challenging questions that will tie fungal community structure to ecosystem function.



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